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TEXT-BOOKS of ANIMAL BIOLOGY a General Zoology of The TEXT-BOOKS OF ANIMAL BIOLOGY * Edited by JULIAN S. HUXLEY, F.R.S. A General Zoology of the Invertebrates by G. S. Carter Vertebrate Zoology by G. R. de Beer Comparative Physiology by L. T. Hogben Animal Ecology by Challes Elton Life in Inland Waters by Kathleen Carpenter The Development of Sex in Vertebrates by F. W. Rogers Brambell * Edited by H. MUNRO Fox, F.R.S. Animal Evolution / by G. S. Carter Zoogeography of the Land and Inland Waters by L. F. de Beaufort Parasitism and Symbiosis by M. Caullery PARASITISM AND ~SYMBIOSIS BY MAURICE CAULLERY Translated by Averil M. Lysaght, M.Sc., Ph.D. SIDGWICK AND JACKSON LIMITED LONDON First Published 1952 !.lADE AND PRINTED IN GREAT BRITAIN BY WILLIAM CLOWES AND SONS, LlMITED, LONDON AND BECCLES CONTENTS LIST OF ILLUSTRATIONS vii PREFACE TO THE ENGLISH EDITION xi CHAPTER I Commensalism Introduction-commensalism in marine animals-fishes and sea anemones-associations on coral reefs-widespread nature of these relationships-hermit crabs and their associates CHAPTER II Commensalism in Terrestrial Animals Commensals of ants and termites-morphological modifications in symphiles-ants.and slavery-myrmecophilous plants . 16 CHAPTER III From Commensalism to Inquilinism and Parasitism Inquilinism-epizoites-intermittent parasites-general nature of modifications produced by parasitism 30 CHAPTER IV Adaptations to Parasitism in Annelids and Molluscs Polychates-molluscs; lamellibranchs; gastropods 40 CHAPTER V Adaptation to Parasitism in the Crustacea Isopoda-families of Epicarida-Rhizocephala-Ascothoracica -Copepoda 65 CHAPTER VI Temporary Parasitism Monstrillida - Orthonectida - Eunicida - Unionida - Gor- dian worms~entomophagous insects 108 CHAPTER VII Parasites which change their Host Cestoda - Cestodaria - Trematoda - Nematoda - Acantho- cephala-Pentastomida-Protozoa-parasitic plants 127 v vi CONTENTS CHAPTER VIII Adaptive Modifications in the Reproduction of Parasites Hermaphroditism and change 'Of sex-increase in egg numbers- accessory reproductive phases-discussion 154 CHAPTER IX Specificity in Parasites and Modes of Host Infestation Strict specificity-modified specificity-trophic prophylaxis-host parasite equilibrium-relative specificity-specificity and access to the host-myiases-hereditary transmission 171 CHAPTER X Reciprocal Reactions of Parasite and Host Parasites and foreign bodies-phagocytosis in normal and abnormal parasites-parasites and toxins-the effect of the parasite on the general metabolism of the host-parasitic castra­ tion-special cases of reaction of hosts to parasites-gall forma- tiM 1~ CHAPTER XI Symbiosis between Animals and Plants Introduction-symbiosis in animals and plants-ectosymbiosis­ ants and fungi-termites and fungi-endosymbiosis-protozoa and intestinal bacteria-termites and flagellates-ruminants and infusoria-zoochlorella! and zooxanthella!-mycetomes of insects -bloodsucking animals-animal luminescence-experimental research on symbiosis 217 CHAPTER XII Symbiosis in Plants Lichens-myxomycetes-myxobacteria-mycorrhiza 256 CHAPTER XIII Is Symbiosis a Primordial Characteristic of the Cell ? BIBLIOGRAPHY 277 INDEX 287 LIST OF ILLUSTRATIONS Aspidosiphon and Heteropsammia cochlea 6 2 Hermit crab in an artificial glass shell, with its commensal Nereilepas Jucata coming out to take part in a meal of sea urchin ovary 8 3 Association of Eupagurus prideauxi and Adamsia palliata. 11 4 Melia tesselata holding a sea anemone in each of its chela: 13 5 Insects that live as commensals with ants 20 6 Larva of Pachycondyla vorax bearing a larva of Metopina pachycondyke 21 7 Head and mandibles of workers of Polyergus ruJescens and of Formica Jusca . 26 8 Ichthyotomus sanguinarius attached to the fin of Myrus vulgaris . 41 9 The stylets forming the organ of fixation in Ichthyotomus . 41 10 Ellobiophrya donacis 42 11 Anterior region of Ichthyotomus 43 12. Thyca stellasteris and T. ectoconcha 50 13 Mucronalia palmipedis 52 14 Anatomy of Stylifer linckice . 54 15 Gasterosiphon deimatis 55 16 Structure of Entocolax, Entoconcha and Enteroxenos 58 17 Entoconcha mirabilis and its relationships with the host 59 18 Part of the gut of Stichopus bearing individuals of Enter- oxenos of various sizes 60 19 Veliger larva of Entoconcha 61 20 Pcedophoropus dicfElobius 63 21 Gnathia maxillaris 67 22 Epicarid larva of Cancricepon elegans 69 23 Microniscus stage, on Calanus elongatus 70 24 Cepon elegans,' cryptoniscan larva and adult dwarf male 71 25 Bopyrus Jougerouxi, a parasite of Leander serratus '. 73 26 Cepon elegans,' adult female . 74 27 An adult entoniscid, Portunion mcenadis, in its normal posi- tion inside the carapace of Carcinus mcenas 77 vii Vlll LIST OF ILLUSTRATIONS 28 Portunion manadis. Stages of development in the crab Carcinus manas 78 29 Portunion manadis: very young female at the beginning of its metamorphosis (asticot stage) . 79 30 Portunion kossmanni: adult female with the brood pouch filled with embryos 79 31 Portunion kossmanni: adult male greatly enlarged 80 32 Epicarids of the family Dajidre 82 33 Ancyroniscus bonnieri: sub-adult female before egg de- position; adult female after laying 84 34 Crab carrying Sacculina, showing the root system 86 35 Larval development of Sacculina . 88 36 J nternal stage of Sacculina 90 37 Thompsonia sp. on Synalpheus brucei 91 38 Cypris larva of Myriocladus 95 39 A. Fragment of the stem of Metacrinus rotundus bearing two females of Synagoga metacrinicola; B. Female of Syna- goga metacrinicola with half the carapace removed 96 40 Laura gerardim 98 41 Baccalaureus japonicus, female 99 42 Baccalaureus japonicus, male 100 43 Myriocladus okadai, female . 102 44 Myriocladus okadai, male 103 45 Xenocr.eloma brl/mpti attached to Polycirrus arenivorus 106 46 Monstrillid parasite in the dorsal vessel of Syllis gracilis. 109 47 Development of some Monstrillidre 111 48 Developmental cycle of Rhopalura ophiocomm 114 49 G10chidium larva 116 50 Primary larvre of various entomophagous Hymenoptera 125 51 Larval forms of Bothriocephalus latus 130 52 Caryophyllaus laticeps, a parasite in the gut of the carp 133 53 Miracidium of Parorchis avitus, a parasite of the gull Larus argenta/us . 137 54 Schistosoma hmmatobium 140 55 Development of Schistosoma mansoni 141 56 Cycle of Porospora portunidarum . 146 57 Developmental cycle of Plasmodium cynomolgi 149 58 Dwarf males parasitizing females in the Ceratioidea 157 LIST OF ILLUSTRATIONS ix )Y 8phcerularia bombi 159 60 Gyrodactylus elegans 164 61 Polyembryony in Encyrtus fuscicollis 166 62 Lithocystis schneideri . 194 63 Modifications in the abdomen of Carcinus mamas under the influence of Sacculina 201 64 The abdomen of Inachus mauritanicus showing modifica- tions due to Sacculina 202 65 Cellular reactions of the host to coccidIa and gregarines . 206 66 A. Fragment of the test of Phormosoma uranus with numer- ous prominent spherical galls of Pionodesmotes phormo- somce; B. Interior aspect of one of the galls . 209 67 Longitudinal section of the root of a melon attacked by Heterodera radicicola . 211 70 Ciliates in the paunch of ruminants 227 71 Larva of a green-fly, Drepanosiphum platanoides, showing the green body or mycetome 236 72 Symbiotic yeasts and mycetocytes in Homoptera 237 73 Sections of luminous organs in Rondeletia minor and Sepiola intermedia 247 74 Cells of luminous tissue from Pyrosoma giganteum with photogenic bacteria 250 75 LarVa! of Sitodrepa panicea ten weeks old 253 76 Louse, Pediculus humanus capitis, female 255 77 Intracellular termination (arbusc1e and sporangioles) of an endotrophic mycorrhiza in Allium sphcerocephalum . 264 78 Seedling of Phalcenopsis grown in a sterile tube by being sown on cotton wool steeped in a decoction of salep with Rhizoctonia mucoroides 267 79 Lelio-Cattleya sown in sterile tubes inoculated with Rhizoctonia of increasing activity . 272 80 Section of a germinating Odontoglossum, showing the penetration of the suspensor after one month, and the intra­ cellular coiling' of Rhizoctonia lanuginosa, as well as its destruction by phagocytosis 273 PREFACE TO THE ENGLISH EDITION IN the present work I have dealt with parasitism from the point of view of general biology. Parasitism is a relationship of direct and limited importance between two organisms, each usually having a clearly defined role, either of host or parasite; the parasite lives at the expense of the host. It is really a special case of the relationship of every organism to its environment, in this instance to another organism, an association which is particularly precise. There exist other associations between organisms, less restricted-but which are also very often specific-that are described as commensalism and mutualism. There are others again which are, on the contrary, more restricted, more constant and less unilateral, to which the name symbiosis has been given. Commensalism, parasitism and symbiosis are man-made categories which in nature are not discontinuous but are really different aspects of the same general laws. This book seeks to make this clear by reviewing these types of association one by one, within the framework of the theory of evolution. Ignorant as we still are of the mecha­ nisms by which evolution is brought about, its reality cannot easily be controverted, and it imposes itself on us more and more as our knowledge increases. Parasites are perhaps the org<lonisms in which this is most evident. In effect they are closely adapted to the very peculiar conditions in which they live, and their organization, specialized as it may be, always appears not like that of autonomous types forming
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